The skimmed milk proteome of dairy cows is affected by the stage of lactation and by supplementation with polyunsaturated fatty acids

Bagwe, S., Tharappel, L. J., Kaur, G. & Buttar, H. S. Bovine colostrum: An emerging nutraceutical. J. Complement. Integr. Med. 12, 175–185. https://doi.org/10.1515/jcim-2014-0039 (2015).Article 
PubMed 

Google Scholar 
Blum, J. W. & Hammon, H. Colostrum effects on the gastrointestinal tract, and on nutritional, endocrine and metabolic parameters in neonatal calves. Livest. Prod. Sci. 66, 151–159. https://doi.org/10.1016/S0301-6226(00)00222-0 (2000).Article 

Google Scholar 
Bigler, N. A., Bruckmaier, R. M. & Gross, J. J. Implications of placentation type on species-specific colostrum properties in mammals. J. Anim. Sci. 100. https://doi.org/10.1093/jas/skac287 (2022).Marnila, P. & Korhonen, H. in Encyclopedia of Dairy Sciences (ed Hubert Roginski) 1950–1956 (Elsevier, 2002).Puppel, K. et al. Composition and factors affecting quality of bovine colostrum: A review. Animals (Basel). 9. https://doi.org/10.3390/ani9121070 (2019).Westhoff, T. A., Borchardt, S. & Mann, S. INVITED REVIEW: Nutritional and management factors that influence colostrum production and composition in dairy cows. J. Dairy Sci.https://doi.org/10.3168/jds.2023-24349 (2024).Article 
PubMed 

Google Scholar 
Nissen, A., Andersen, P. H., Bendixen, E., Ingvartsen, K. L. & Røntved, C. M. Colostrum and milk protein rankings and ratios of importance to neonatal calf health using a proteomics approach. J. Dairy Sci. 100, 2711–2728. https://doi.org/10.3168/jds.2016-11722 (2017).Article 
PubMed 

Google Scholar 
Fahey, M. J., Fischer, A. J., Steele, M. A. & Greenwood, S. L. Characterization of the colostrum and transition milk proteomes from primiparous and multiparous holstein dairy cows. J. Dairy Sci. 103, 1993–2005. https://doi.org/10.3168/jds.2019-17094 (2020).Article 
PubMed 

Google Scholar 
Feng, Z. et al. Unravelling the proteomic profiles of bovine colostrum and mature milk derived from the first and second lactations. Foods (Basel Switzerland) 12. https://doi.org/10.3390/foods12224056 (2023).Delosière, M., Pires, J., Bernard, L., Cassar-Malek, I. & Bonnet, M. Milk proteome from in silico data aggregation allows the identification of putative biomarkers of negative energy balance in dairy cows. Sci. Rep. 9, 9718. https://doi.org/10.1038/s41598-019-46142-7 (2019).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Veshkini, A., Ceciliani, F., Bonnet, M. & Hammon, H. M. Review: Effect of essential fatty acids and conjugated linoleic acid on the adaptive physiology of dairy cows during the transition period. Animal 17, 100757. https://doi.org/10.1016/j.Animal.2023.100757 (2023).Article 
PubMed 

Google Scholar 
Moallem, U. Invited review: Roles of dietary n-3 fatty acids in performance, milk fat composition, and reproductive and immune systems in dairy cattle. J. Dairy Sci. 101, 8641–8661. https://doi.org/10.3168/jds.2018-14772 (2018).Article 
PubMed 

Google Scholar 
Bauman, D. E. & Griinari, J. M. Regulation and nutritional manipulation of milk fat: Low-fat milk syndrome. Livest. Prod. Sci. 70, 15–29. https://doi.org/10.1016/S0301-6226(01)00195-6 (2001).Article 

Google Scholar 
Vogel, L. et al. Effects of abomasal infusion of essential fatty acids together with conjugated linoleic acid in late and early lactation on performance, milk and body composition, and plasma metabolites in dairy cows. J. Dairy Sci. 103, 7431–7450. https://doi.org/10.3168/jds.2019-18065 (2020).Article 
PubMed 

Google Scholar 
Xing, Z. Y. et al. Short communication: A decrease in diameter of milk fat globules accompanies milk fat depression induced by conjugated linoleic acid supplementation in lactating dairy cows. J. Dairy Sci. 103, 5143–5147. https://doi.org/10.3168/jds.2019-17845 (2020).Article 
PubMed 

Google Scholar 
Lönnerdal, B. Bioactive proteins in human milk: Health, nutrition, and Implications for infant formulas. J. Pediatr. 173, S4–S9. https://doi.org/10.1016/j.jpeds.2016.02.070 (2016).Article 
PubMed 

Google Scholar 
Huang, Q. X. et al. Milk fat globule membrane proteins are involved in controlling the size of milk fat globules during conjugated linoleic acid–induced milk fat depression. J. Dairy Sci. 105, 9179–9190. https://doi.org/10.3168/jds.2022-22131 (2022).Article 
PubMed 

Google Scholar 
Moallem, U. Invited review: Roles of dietary n-3 fatty acids in performance, milk fat composition, and reproductive and immune systems in dairy cattle. J. Dairy Sci. 101, 8641–8661. https://doi.org/10.3168/jds.2018-14772 (2018).Article 
PubMed 

Google Scholar 
Uken, K. L. et al. Modulation of colostrum composition and fatty acid status in neonatal calves by maternal supplementation with essential fatty acids and conjugated linoleic acid starting in late lactation. J. Dairy Sci. 104, 4950–4969. https://doi.org/10.3168/jds.2020-19627 (2021).Article 
PubMed 

Google Scholar 
Ferlay, A., Doreau, M., Martin, C. & Chilliard, Y. Effects of incremental amounts of extruded linseed on the milk fatty acid composition of dairy cows receiving hay or corn silage. JDS 96, 6577–6595. https://doi.org/10.3168/jds.2013-6562 (2013).Article 

Google Scholar 
Petit, H. V., Germiquet, C. & Lebel, D. Effect of feeding whole, unprocessed sunflower seeds and flaxseed on milk production, milk composition, and prostaglandin secretion in dairy cows <s up>1</sup>. J. Dairy Sci. 87, 3889–3898. https://doi.org/10.3168/jds.S0022-0302(04)73528-6 (2004).Article 
PubMed 

Google Scholar 
Hötger, K. et al. Supplementation of conjugated linoleic acid in dairy cows reduces endogenous glucose production during early lactation1. J. Dairy Sci. 96, 2258–2270. https://doi.org/10.3168/jds.2012-6127 (2013).Article 
PubMed 

Google Scholar 
Kowalski, Z. M., Górka, P., Micek, P., Oprządek, J. & Tröscher, A. Effects of Rumen-protected conjugated linoleic acid (CLA) on performance of primiparous and multiparous cows in the transition period. J. Anim. Feed Sci. 28, 220–229. https://doi.org/10.22358/jafs/110083/2019 (2019).Article 

Google Scholar 
Qin, N. et al. Dietary supplement of conjugated linoleic acids or polyunsaturated fatty acids suppressed the mobilization of body fat reserves in dairy cows at early lactation through different pathways. J. Dairy Sci. 101, 7954–7970. https://doi.org/10.3168/jds.2017-14298 (2018).Article 
PubMed 

Google Scholar 
Moore, C. E. et al. Increasing amounts of conjugated linoleic acid (CLA) progressively reduces milk fat synthesis immediately postpartum. J. Dairy Sci. 87, 1886–1895. https://doi.org/10.3168/jds.S0022-0302(04)73347-0 (2004).Article 
PubMed 

Google Scholar 
Vincent, D., Elkins, A., Condina, M. R., Ezernieks, V. & Rochfort, S. Quantitation and identification of intact major milk proteins for high-throughput LC-ESI-Q-TOF MS analyses. PLoS One. 11, e0163471. https://doi.org/10.1371/journal.pone.0163471 (2016).Article 
PubMed 
PubMed Central 

Google Scholar 
Delosière, M., Bernard, L., Viala, D., Fougère, H. & Bonnet, M. Milk and plasma proteomes from cows facing diet-induced milk fat depression are related to immunity, lipid metabolism and inflammation. Animal 17, 100822. https://doi.org/10.1016/j.animal.2023.100822 (2023).Article 

Google Scholar 
Scuderi, R. A. et al. Comparative analysis of the skim milk and milk fat globule membrane proteomes produced by Jersey cows grazing pastures with different plant species diversity. J. Dairy Sci. 103, 7498–7508. https://doi.org/10.3168/jds.2019-17726 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Greenwood, S. L. & Honan, M. C. Symposium review: Characterization of the bovine milk protein profile using proteomic techniques. J. Dairy Sci. 102, 2796–2806. https://doi.org/10.3168/jds.2018-15266 (2019).Article 

Google Scholar 
Georgiadi, A. & Kersten, S. Mechanisms of gene regulation by fatty acids. Adv. Nutr. 3, 127–134. https://doi.org/10.3945/an.111.001602 (2012).Article 
PubMed 
PubMed Central 

Google Scholar 
Foley, J. & Otterby, D. Availability, storage, treatment, composition, and feeding value of surplus colostrum: A review. J. Dairy Sci. 61, 1033–1060. https://doi.org/10.3168/jds.S0022-0302(78)83686-8 (1978).Article 

Google Scholar 
Liermann, W. et al. Effects of a maternal essential fatty acid and conjugated linoleic acid supplementation during late pregnancy and early lactation on hematologic and immunological traits and the oxidative and anti-oxidative status in blood plasma of neonatal calves. Animal (Basel) 11, 2168. https://doi.org/10.3390/ani11082168 (2021).Article 

Google Scholar 
Zhang, L. et al. Bovine milk proteome in the first 9 days: Protein interactions in maturation of the immune and digestive system of the newborn. PLoS One 10, e0116710. https://doi.org/10.1371/journal.pone.0116710 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Hartl, F. U. & Hayer-Hartl, M. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 16, 574–581. https://doi.org/10.1038/nsmb.1591 (2009).Article 
PubMed 

Google Scholar 
Liu, Y. et al. GRP78 regulates milk biosynthesis and the proliferation of bovinemammaryepithelial cells through the mTOR signaling pathway. Cell. Mol. Biol. Lett. 24, 57. https://doi.org/10.1186/s11658-019-0181-x (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Arslan, A. et al. Bovine colostrum and its potential for human health and nutrition. Front. Nutr. 8. https://doi.org/10.3389/fnut.2021.651721 (2021).Saporito-Magriña, C., Facio, M. L., Lopez-Montañana, L., Pagano, G. & Repetto, M. G. Copper-induced aggregation of IgG: A potential driving force for the formation of circulating protein aggregates. Metallomics: Integr. Biometal Sci. 15. https://doi.org/10.1093/mtomcs/mfad005 (2023).Goff, J. P. Invited review: Mineral absorption mechanisms, mineral interactions that affect acid-base and antioxidant status, and diet considerations to improve mineral status. J. Dairy Sci. 101, 2763–2813. https://doi.org/10.3168/jds.2017-13112 (2018).Article 
PubMed 

Google Scholar 
Hammon, H. M., Liermann, W., Frieten, D., & Koch, C. Review: Importance of colostrum supply and milk feeding intensity on gastrointestinal and systemic development in calves. Animal. 14, s133–s143. https://doi.org/10.1017/S1751731119003148 (2020).Article 
PubMed 

Google Scholar 
Stott, G. H., Marx, D. B., Menefee, B. E. & Nightengale, G. T. Colostral immunoglobulin transfer in calves II. The rate of absorption. J. Dairy Sci. 62, 1766–1773. https://doi.org/10.3168/jds.S0022-0302(79)83495-5 (1979).Article 
PubMed 

Google Scholar 
Hammon, H. M., Steinhoff-Wagner, J., Flor, J., Schönhusen, U. & Metges, C. C. LACTATION BIOLOGY SYMPOSIUM: Role of colostrum and colostrum components on glucose metabolism in neonatal calves1,2. J. Anim. Sci. 91, 685–695. https://doi.org/10.2527/jas.2012-5758 (2013).Article 
PubMed 

Google Scholar 
Sharma, S. et al. Lactoperoxidase: Structural insights into the function,ligand binding and inhibition. Int. J. Biochem. Mol. Biol. 4, 108–128 (2013).PubMed 
PubMed Central 

Google Scholar 
Ahrné, L. & Björck, L. Lipolysis and the distribution of lipase activity in bovine milk in relation to stage of lactation and time of milking. J. Dairy Res.Bold”>52, 55–64. https://doi.org/10.1017/s002202990002389x (1985).Article 
PubMed 

Google Scholar 
McGrath, B. A., Fox, P. F., McSweeney, P. L. H. & Kelly, A. L. Composition and properties of bovine colostrum: A review. Dairy Sci. Technol. 96, 133–158. https://doi.org/10.1007/s13594-015-0258-x (2016).Article 

Google Scholar 
Manoni, M., Di Lorenzo, C., Ottoboni, M., Tretola, M. & Pinotti, L. Comparative proteomics of milk fat globule membrane (MFGM) proteome across species and lactation stages and the potentials of MFGM fractions in infant formula preparation. Foods (Basel Switzerland) 9. https://doi.org/10.3390/foods9091251 (2020).Sats, A. et al. Bovine colostrum: Postpartum changes in fat globule size distribution and fatty acid profile. J. Dairy Sci. 105, 3846–3860. https://doi.org/10.3168/jds.2021-20420 (2022).Article 
PubMed 

Google Scholar 
Dickow, J. A., Larsen, L. B., Hammershøj, M. & Wiking, L. Cooling causes changes in the distribution of lipoprotein lipase and milk fat globule membrane proteins between the skim milk and cream phase. J. Dairy Sci. 94, 646–656. https://doi.org/10.3168/jds.2010-3549 (2011).Article 
PubMed 

Google Scholar 
Cartier, P. & Chilliard, Y. Spontaneous lipolysis in bovine milk: Combined effects of nine characteristics in native milk. J. Dairy Sci.Bold”>73, 1178–1186. https://doi.org/10.3168/jds.S0022-0302(90)78780-2 (1990).Article 

Google Scholar 
Bonnet, M., Leroux, C., Chilliard, Y. & Martin, P. Rapid communication: Nucleotide sequence of the ovine lipoprotein lipase cDNA. J. Anim. Sci.-Menasha Then Albany Then Champaign Illinois 78, 2994–2995 (2000).
Google Scholar 
Delosière, M. et al. Protein signatures of spontaneous lipolysis and lipoprotein lipase activity in cow’s milk. J. Proteom. 285, 104951. https://doi.org/10.1016/j.jprot.2023.104951 (2023).Article 

Google Scholar 
Beswick, N. S. & Kennelly, J. J. Influence of bovine growth hormone and growth hormone-releasing factor on messenger RNA abundance of lipoprotein lipase and stearoyl-CoA desaturase in the bovine mammary gland and adipose tissue. J. Anim. Sci. 78, 412–419. https://doi.org/10.2527/2000.782412x (2000).Article 
PubMed 

Google Scholar 
Mani, O., Sorensen, M., Sejrsen, K., Bruckmaier, R. & Albrecht, C. Differential expression and localization of lipid transporters in the bovine mammary gland during the pregnancy-lactation cycle. J. Dairy Sci. 92, 3744–3756. https://doi.org/10.3168/jds.2009-2063 (2009).Article 
PubMed 

Google Scholar 
Liu, L. et al. Regulation of peroxisome proliferator-activated receptor gamma on milk fat synthesis in dairy cow mammary epithelial cells. In Vitro Cell. Dev. Biol.-Anim.. 52, 1044–1059. https://doi.org/10.1007/s11626-016-0059-4 (2016).Article 
PubMed 

Google Scholar 
Tian, Z. et al. Transcriptional regulation of milk fat synthesis in dairy cattle. J. Funct. Foods. 96, 105208. https://doi.org/10.1016/j.jff.2022.105208 (2022).Article 

Google Scholar 
Mather, I. H. A review and proposed nomenclature for major proteins of the milk-fat globule membrane1,2. J. Dairy Sci. 83, 203–247. https://doi.org/10.3168/jds.S0022-0302(00)74870-3 (2000).Article 
PubMed 

Google Scholar 
McManaman, J. Formation of milk lipids: A molecular perspective. Clin. Lipidol. 4, 391–401. https://doi.org/10.2217/clp.09.15 (2009).Article 
PubMed 
PubMed Central 

Google Scholar 
Uken, K. L. et al. Effect of maternal supplementation with essential fatty acids and conjugated linoleic acid on metabolic and endocrine development in neonatal calves. J. Dairy Sci. 104, 7295–7314. https://doi.org/10.3168/jds.2020-20039 (2021).Article 
PubMed 

Google Scholar 
Liermann, W. et al. Influences of maternal conjugated linoleic acid and essential fatty acid supply during late pregnancy and early lactation on T and B cell subsets in Mesenteric Lymph Nodes and the small intestine of neonatal calves. Front. Veterinary Sci. 7https://doi.org/10.3389/fvets.2020.604452 (2020).Liermann, W. et al. Effects of a maternal essential fatty acid and conjugated linoleic acid supplementation during late pregnancy and early lactation on hematologic and immunological traits and the oxidative and anti-oxidative status in blood plasma of neonatal calves. Animal (Basel) 11. https://doi.org/10.3390/ani11082168 (2021).Liermann, W. et al. Maternal conjugated linoleic acid supply in combination with or without essential fatty acids during late pregnancy and early lactation: Investigations on physico-chemical characteristics of the jejunal content and jejunal microbiota in neonatal calves. Front. Vet. Sci.Bold”>9, 839860. https://doi.org/10.3389/fvets.2022.839860 (2022).Article 
PubMed 
PubMed Central 

Google Scholar 
Blasiole, D. A., Davis, R. A. & Attie, A. D. The physiological and molecular regulation of lipoprotein assembly and secretion. Mol. Biosyst. 3, 608–619. https://doi.org/10.1039/b700706j (2007).Article 
PubMed 

Google Scholar 
Jia, W., Zhang, R., Zhu, Z. & Shi, L. A. High-throughput comparative proteomics of milk fat globule membrane reveals breed and lactation stages specific variation in protein abundance and functional differences between milk of saanen dairy goat and Holstein bovine. Front. Nutr. 8, 680683. https://doi.org/10.3389/fnut.2021.680683 (2021).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Mu, T. et al. Regulation of key genes for milk Fat Synthesis in ruminants. Front. Nutr. 8. https://doi.org/10.3389/fnut.2021.765147 (2021).Melchior, J. T. et al. Apolipoprotein A-I modulates HDL particle size in the absence of apolipoprotein A-II. J. Lipid Res. 62, 100099. https://doi.org/10.1016/j.jlr.2021.100099 (2021).Article 
PubMed 
PubMed Central 

Google Scholar 
Sandri, E. C., Camêra, M., Sandri, E. M., Harvatine, K. J. & De Oliveira, D. E. Peroxisome proliferator-activated receptor gamma (PPARγ) agonist fails to overcome trans-10, cis-12 conjugated linoleic acid (CLA) inhibition of milk fat in dairy sheep. Animal 12, 1405–1412. https://doi.org/10.1017/s1751731117002956 (2018).Article 
PubMed 

Google Scholar 
Suárez-Vega, A. et al. Conjugated linoleic acid (CLA)-induced milk fat depression: Application of RNA-Seq technology to elucidate mammary gene regulation in dairy ewes. Sci. Rep. 9, 4473. https://doi.org/10.1038/s41598-019-40881-3 (2019).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
van Diepen, J. A. et al. PPAR-alpha dependent regulation of vanin-1 mediates hepatic lipid metabolism. J. Hepatol. 61, 366–372. https://doi.org/10.1016/j.jhep.2014.04.013 (2014).Article 
PubMed 

Google Scholar 
Drover, V. A. & Abumrad, N. A. CD36-dependent fatty acid uptake regulates expression of peroxisome proliferator activated receptors. Biochem. Soc. Trans. 33, 311–315. https://doi.org/10.1042/bst0330311 (2005).Article 
PubMed 

Google Scholar 
GFE. GfE; Gesellschaft für Ernährungsphysiologie (German Society of Nutrition Physiology). Empfehlungen zur Energie- und Nährstoffversorgung der Milchkühe und Aufzuchtrinder (Recommended energy and nutrient suply of dairy cows and growing cattle). Vol. 8. DLGVerlag, Frankfurt a. M., Germany (2001).GFE. GfE; Gesellschaft für Ernährungsphysiologie (German Society of Nutrition Physiology). New equations for predicting metabolisable energy of grass and maize products for ruminants. Communications of the Committee for Requirement Standards of the Society of Nutrition Physiology. Proc. Soc. Nutr. Physiol. 17, 191–198 (2008).GFE. GfE; Gesellschaft für Ernährungsphysiologie (German Society of Nutrition Physiology). New equations for predicting metabolisable energy of compound feeds for cattle. Communications of the Committee for Requirement Standards of the Society of Nutrition Physiology. Proc. Soc. Nutr. Physiol. 18, 143–146 (2009).DLG. DLG (Deutsche Landwirtschafts-Gesellschaft, German Agricultural Society. ). Leitfaden zur Berechnung des Energiegehaltes bei Einzel-und Mischfuttermitteln für die Schweine-und Rinderfütterung (Guidelines for calculation of energy content of single and mixed feedstuff for pigs and cattle). Stellungnahme des DLG-Arbeitskreises Futter und Fütterung (2013).Boschetti, E. & Righetti, P. G. The ProteoMiner in the proteomic arena: A non-depleting tool for discovering low-abundance species. J. Proteom. 71, 255–264. https://doi.org/10.1016/j.jprot.2008.05.002 (2008).Article 

Google Scholar 
Veshkini, A. et al. Plasma proteomics reveals crosstalk between lipid metabolism and immunity in dairy cows receiving essential fatty acids and conjugated linoleic acid. Sci. Rep. 12, 5648. https://doi.org/10.1038/s41598-022-09437-w (2022).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Veshkini, A. et al. Liver proteome profiling in dairy cows during the transition from gestation to lactation: Effects of supplementation with essential fatty acids and conjugated linoleic acids as explored by PLS-DA. J. Proteom. 252, 104436. https://doi.org/10.1016/j.jprot.2021.104436 (2022).Article 

Google Scholar 
Liquet, B., Cao, K. A. L., Hocini, H. & Thiébaut, R. A novel approach for biomarker selection and the integration of repeated measures experiments from two assays. BMC Bioinform. 13, 325. https://doi.org/10.1186/1471-2105-13-325 (2012).Article 

Google Scholar 
Westerhuis, J. A., van Velzen, E. J., Hoefsloot, H. C. & Smilde, A. K. Multivariate paired data analysis: Multilevel PLSDA versus OPLSDA. Metabolomics 6, 119–128. https://doi.org/10.1007/s11306-009-0185-z (2010).Article 
PubMed 

Google Scholar 
He, F. & Maslov, S. Pan-and core-network analysis of co-expression genes in a model plant. Sci. Rep. 6, 38956. https://doi.org/10.1038/srep38956 (2016).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar